TY - JOUR
T1 - Robust banded protoxylem pattern formation through microtubule-based directional ROP diffusion restriction
AU - Jacobs, Bas
AU - Molenaar, Jaap
AU - Deinum, Eva E.
PY - 2020/10/7
Y1 - 2020/10/7
N2 - In plant vascular tissue development, different cell wall patterns are formed, offering different mechanical properties optimised for different growth stages. Critical in these patterning processes are Rho of Plants (ROP) proteins, a class of evolutionarily conserved small GTPase proteins responsible for local membrane domain formation in many organisms. While te spotted metaxylem pattern can easily be understood as a result of a Turing-style reaction-diffusion mechanism, it remains an open question how the consistent orientation of evenly spaced bands and spirals as found in protoxylem is achieved. We hypothesise that this orientation results from an interaction between ROPs and an array of transversely oriented cortical microtubules that acts as a directional diffusion barrier. Here, we explore this hypothesis using partial differential equation models with anisotropic ROP diffusion and show that a horizontal microtubule array acting as a vertical diffusion barrier to active ROP can yield a horizontally banded ROP pattern. We then study the underlying mechanism in more detail, finding that it can only orient curved pattern features but not straight lines. This implies that, once formed, banded and spiral patterns cannot be reoriented by this mechanism. Finally, we observe that ROPs and microtubules together only form ultimately static patterns if the interaction is implemented with sufficient biological realism.
AB - In plant vascular tissue development, different cell wall patterns are formed, offering different mechanical properties optimised for different growth stages. Critical in these patterning processes are Rho of Plants (ROP) proteins, a class of evolutionarily conserved small GTPase proteins responsible for local membrane domain formation in many organisms. While te spotted metaxylem pattern can easily be understood as a result of a Turing-style reaction-diffusion mechanism, it remains an open question how the consistent orientation of evenly spaced bands and spirals as found in protoxylem is achieved. We hypothesise that this orientation results from an interaction between ROPs and an array of transversely oriented cortical microtubules that acts as a directional diffusion barrier. Here, we explore this hypothesis using partial differential equation models with anisotropic ROP diffusion and show that a horizontal microtubule array acting as a vertical diffusion barrier to active ROP can yield a horizontally banded ROP pattern. We then study the underlying mechanism in more detail, finding that it can only orient curved pattern features but not straight lines. This implies that, once formed, banded and spiral patterns cannot be reoriented by this mechanism. Finally, we observe that ROPs and microtubules together only form ultimately static patterns if the interaction is implemented with sufficient biological realism.
KW - Anisotropic diffusion
KW - Partial differential equations
KW - ROP patterning
U2 - 10.1016/j.jtbi.2020.110351
DO - 10.1016/j.jtbi.2020.110351
M3 - Article
C2 - 32505828
AN - SCOPUS:85087001808
SN - 0022-5193
VL - 502
JO - Journal of Theoretical Biology
JF - Journal of Theoretical Biology
M1 - 110351
ER -